A distinct transcriptome characterizes neural crest-derived cells at the migratory wavefront during enteric nervous system development

Author:

Stavely Rhian1,Hotta Ryo1ORCID,Guyer Richard A.1ORCID,Picard Nicole1,Rahman Ahmed A.1,Omer Meredith1,Soos Adam2ORCID,Szocs Emoke2,Mueller Jessica1,Goldstein Allan M.1ORCID,Nagy Nandor2ORCID

Affiliation:

1. Pediatric Surgery Research Laboratories, Massachusetts General Hospital, Harvard Medical School 1 Department of Pediatric Surgery , , Boston, MA 02114 , USA

2. Faculty of Medicine, Semmelweis University 2 Department of Anatomy, Histology and Embryology , , Budapest 1094, Hungary

Abstract

ABSTRACTEnteric nervous system development relies on intestinal colonization by enteric neural crest-derived cells (ENCDCs). This is driven by a population of highly migratory and proliferative ENCDCs at the wavefront, but the molecular characteristics of these cells are unknown. ENCDCs from the wavefront and the trailing region were isolated and subjected to RNA-seq. Wavefront-ENCDCs were transcriptionally distinct from trailing ENCDCs, and temporal modelling confirmed their relative immaturity. This population of ENCDCs exhibited altered expression of ECM and cytoskeletal genes, consistent with a migratory phenotype. Unlike trailing ENCDCs, the wavefront lacked expression of genes related to neuronal or glial maturation. As wavefront ENCDC genes were associated with migration and developmental immaturity, the genes that remain expressed in later progenitor populations may be particularly pertinent to understanding the maintenance of ENCDC progenitor characteristics. Dusp6 expression was specifically upregulated at the wavefront. Inhibiting DUSP6 activity prevented wavefront colonization of the hindgut, and inhibited the migratory ability of post-colonized ENCDCs from midgut and postnatal neurospheres. These effects were reversed by simultaneous inhibition of ERK signaling, indicating that DUSP6-mediated ERK inhibition is required for ENCDC migration in mouse and chick.

Funder

National Institutes of Health

Hungarian Science Foundation

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

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